Alternative electron pathways of photosynthesis drive the algal CO₂ concentrating mechanism

Abstract

Global photosynthesis consumes ten times more CO₂ than net anthropogenic emissions, and microalgae account for nearly half of this consumption¹. The great efficiency of algal photosynthesis relies on a mechanism concentrating CO₂ (CCM) at the catalytic site of the carboxylating enzyme RuBisCO, thus enhancing CO₂ fixation². While many cellular components involved in the transport and sequestration of inorganic carbon (C_i) have been uncovered^3,4, the way microalgae supply energy to concentrate CO₂ against a thermodynamic gradient remains elusive^4-6. Here, by monitoring dissolved CO₂ consumption, unidirectional O₂ exchange and the chlorophyll fluorescence parameter NPQ in the green alga Chlamydomonas, we show that the complementary effects of cyclic electron flow and O₂ photoreduction, respectively mediated by PGRL1 and flavodiiron proteins, generate the proton motive force (pmf) required by C_i transport across thylakoid membranes. We demonstrate that the trans-thylakoid pmf is used by bestrophin-like C_i transporters and further establish that a chloroplast-to-mitochondria electron flow contributes to energize non-thylakoid C_i transporters, most likely by supplying ATP. We propose an integrated view of the CCM energy supply network, describing how algal cells distribute photosynthesis energy to power different C_i transporters, thus paving the way to the transfer of a functional algal CCM in plants towards improving crop productivity.